CAB Reviews 2020 15, No. 026

Alternatives to synthetic pesticides for the management of the banana borer weevil ( sordidus) (Coleoptera: Curculioniidae)

N.J. Okolle1,2*, C. Ngosong3, L.T. Nanganoa4 and L.L. Dopgima5,6

Address: 1Entomology-Nematology Unit, Institute of Agricultural Research for Development (IRAD), Ekona, Southwest Region, Cameroon. 2Laboratory of Entomology & Nematology, African Research Centre on Bananas and Plantains (CARBAP), Njombe, Littoral Region, Cameroon. 3Department of Agronomy and Applied Molecular Sciences, Faculty of Agriculture and Veterinary Medicine, University of Buea, Buea, South West Region, Cameroon. 4Soils Unit, Institute of Agricultural Research for Development (IRAD), Ekona, South West Region, Cameroon. 5Biotechnology Unit, Institute of Agricultural Research for Development (IRAD), Ekona, South West Region, Cameroon. 6Research Service, Delegation of Scientific Research & Innovations, Buea, South West Region, Cameroon.

*Correspondence: Justin Okolle. Email: [email protected]

Received: 5 November 2019 Accepted: 20 March 2020 doi: 10.1079/PAVSNNR202015026

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews

© CAB International 2020 (Online ISSN 1749-8848)

Abstract

Bananas and plantains are important staple crops for many people in developing countries, but these crops are severely affected by biotic constraints that reduce productivity. A major biotic stress is the banana corm borer weevil (C. sordidus) whose larvae eat corm/pseudostem tissues that eventually weaken the plants and cause toppling. To manage these borer weevils, most farmers use synthetic pesticides with active ingredients from different pesticide groups. Over reliance and abusive use of pesticides result in detrimental effects on the environment and human health. These effects together with ecological backlashes such as development of resistance by the have led to numerous advocacies to minimize the use of these chemicals. To achieve this, there has been increasing number of researches to seek sustainable alternatives that could be used to replace these synthetic pesticides or be integrated with less toxic chemicals to effectively manage the pest. This review summarizes global research on the use of synthetic pesticides and alternative management techniques such as the use of appropriate cultural practices (e.g., clean planting materials, fallowing, mulching, intercropping, and trapping), botanical pesticides (e.g., from Solanaceae, Asteraceae, and Meliaceae), entomopathogens, predators/parasitoids, and the use of resistant crop varieties, as well as possibilities of engineering phytocystatins to produce transgenic varieties that will be harmful to weevil. The review ends with conclusions, limitations/gaps, and recommendations for future research for the different alternative options.

Keywords: , pest, integrated pest management

Review methodology: To successfully carry out this review, we collected lots of information from different sources including internet search engines, libraries, consultation of experts from different parts of the world via individual emails, yahoo groups (e.g., pestnet@ yahoogroups.com), and Whatsapp groups. The information collected were mainly primary research (peer-reviewed manuscripts published in journals) as well as scientific reports or articles in conference proceedings or annual reports. Secondary literature especially from news bulletins, magazines, and books were also consulted. Focus on all these was on the banana borer weevil (C. sordidus) and the different management options that have been tested or implemented in the laboratory and/or on the field. The information collected was categorized to form a table of content that guided the write up. Aspects of the content focused on general information on pests of bananas and plantains, bioecology of C. sordidus, and management options (use of synthetic pesticides, cultural practices, biotechnological options—genetic engineered plants/use of resistant varieties, botanicals, microbials, predators/predators, mass trapping/ pheromones, and use of cystatins).

http://www.cabi.org/cabreviews 2 CAB Reviews Introduction Distribution and dispersal

Bananas and plantains (Musa spp.) are cultivated in many The borer weevils occur in fields throughout the year and countries in the world, especially in tropical developing adults are free-living. Among the 28 borer pests associated countries. According to Ploetz et al. [1], these crops rank with bananas and plantains worldwide [23, 24], banana among the world’s most valuable primary agricultural corm weevil borers are most widely distributed [6, 7, 25]. commodities. According to FAO [2], bananas and plantains Generally, adults are negatively phototropic, and are active together serve as a staple food for at least 400 million in the night and are not commonly seen in the fields unless people globally. These food crops have therefore been caught in traps. The adults are usually found in soil around rated as the fourth most valuable food after rice, wheat, mats, within leaf sheaths of living pseudostems and and milk [3]. Bananas and plantains provide about 25% of harvested stumps/corms [8, 17, 26, 27]. Messiaen [26] food-energy requirements for about 70 million people in suggested that movement from and to adjacent fields by Sub-Saharan Africa (SSA) and since the fruits are produced walking is limited. However, Rannestad et al. [28] showed all year round, these crops play an important role in food that the migration potential of banana weevil is greater security and income generation to many resource-poor than previously reported and this should be taken into farmers especially during low production periods of local account when new banana fields are established with clean cash crops like cocoa, coffee, and oil palms [4]. These crops planting materials. are mainly cultivated in backyard gardens, smallholder farms, and commercial plantations that represent a valuable Damage and damage signs/symptoms source of employment to thousands of peoples [5]. Worldwide, the production of Musa spp. is usually Even though adults feed on decomposed corms in banana constrained by biotic factors such as pests and diseases. fields, the larvae usually cause damage. The economic The common pests are corm borer weevils (Cosmopolites importance of borer weevils varies with agroecological sordidus), stem borer weevils (Odoiporus longicollis and region, cultivars, production system, and level of Metamasius spp.), skippers (Erionota thrax and Erionota implementation of crop protection practices. Corm damage torus), lesion nematodes (e.g., Radopholus similis), mealy and percentage of plants attacked in the fields is usually bugs (Pseudococcus spp. and Dysmicoccus spp.), thrips, aphids assessed or estimated using Coefficient of Infestation (CI) (Pentalonia nigronervosa), huntsman spider, red spider mites, of Vilardebo [29] or Percentage Coefficient of Infestation white flies, snails (Limacolaria spp.) while common diseases [26]. Damage is usually assessed by observing the periphery are black sigatoka (Mycosphaerella fijiensis), banana wilt of corms (external damage) and/or the cross section of (Xanthomonas spp.), fusarium wilt (tropical race 4), banana corms, that is, cortex and central cylinder (internal damage). streak viruses, and banana bunchy top [4, 6–13]. Borer Damage in the central cylinder showed greater effect on weevil is the most important pests with serious damage on yield than damage in the cortex in highland cooking banana plantains and usually found in most banana/plantain in Uganda [16]. In addition, corm damage is common in producing zones [4, 14–20]. farms with poor soil nutrient status, inappropriate agronomic practices, and poor phytosanitary measures, with severe damage reported on small-scale plantain farms Brief on the bioecology of C. sordidus compared to commercial plantations [4, 15, 30, 31]. Larvae are the most destructive stage, using their strong mandibles Morphology and life cycle to escavate and create tunnels or galleries in the rhizome (corm) and sometimes extending to the pseudostem. Larval There are three main species of borer weevils that affect feeding usually results in weak growth, poor anchorage and Musa spp. including Cosmopolites sordidus, Metamasius toppling especially during windy periods and infestation is sericeus, and Pollytus mellerborgii, although C. sordidus is the usually low in the first cycle, but increases significantly most economically important. Young adults of C. sordidus during older cycles [32, 33]. Infested plants show stunted are reddish-brown in color while the older ones are dark growth, delayed maturation [34], reduced bunch weight, or black, and adults are slow walkers. The undergoes and can snap or topple [35–37]. holometabolous development and after mating, females use their rostrum to create tiny holes and then lay a single egg in each hole [21]. These eggs are white, oval in shape Population dynamics and may hatch within 5–8 days. Larvae from these eggs pass through 5–6 instars lasting 30–50 days. A mature larva Generally, population dynamics involves changes in is about 10–12 mm long, apodous, creamy white, has dark numbers of an organism as well as the biological and brown and well developed mandibles, as well as a curved environmental processes influencing such changes [38–40]. body [21]. After intense feeding, the larvae undergo a Concerning C. sordidus, the main method used to monitor dramatic change to form pupa. Adult longevity of up to or estimate the population is trapping (pseudostems or about 15 months has been reported in the laboratory [22]. pheromones). The dynamics of this pest varies from one

http://www.cabi.org/cabreviews N.J. Okolle, C. Ngosong, L.T. Nanganoa and L.L. Dopgima 3 country to another, but with some common determinants the management of borer weevils infesting bananas and such as presence of predators, soil type, agronomic plantains. These groups of pesticides include organochlorines practices, farming season, and temperature [4, 17, 26]. (e.g., chlordecone), organophosphates (e.g., chlorpyrifos, terbufos, ethoprofos), carbamates (e.g., carbofuran), pyrethroids (e.g., cypermethrine), neonicotinoids (e.g., Justification/Objective of the review imidacloprid, thiamethoxam), and phenyl pyrazoles (e.g., fipronil) [4, 26, 41, 42, 52–57]. First pesticides used against Cosmopolites sordidus is an important economic pest on the borer weevils were Paris Green and organochlorines such Musa species in the world, especially in smallholder farms. as BHC, dieldrin, lindane, chlordecone, and DDT [58, 59]. To minimize the damage caused by this biotic constraint, Although these were effective, they were persistent and most smallholder farmers often use synthetic pesticides therefore had potential for bioaccumulation and weevils while commercial or agro-industrial plantations mainly were reported to develop resistance against these pesticides integrate cultural techniques with different types of [60]. These led to the use of organophosphates (e.g., synthetic pesticides [4, 41–43]. In addition, these synthetic chlorpyriphos, pirimiphos-ethyl, ethoprofos, terbufos, pesticides are frequently misused, which could be cadusofos, isophenfos), carbamates (e.g., carbufuran, detrimental on the environment and human health, with aldicarbe, oxamyl), and some pyrethroids (e.g., deltamethrine, emergence of ecological backlashes such as resurgence, bifenthrine and zeta-cypermethrine) [4, 10, 41, 43, 61–65]. replacement, and resistance [44–49]. Based on these over With the continuous development of resistance of the reliance and misuse of synthetic pesticides, there has been weevils to organophosphates, carbamates, and pyrethroids, global advocacy to minimize their use for crop protection new formulations have been developed and tested including and to increase the search for sustainable alternatives, the neonicotinoids and phenyl pyrazoles that are commonly especially for the highly hazardous pesticides [44, 50, 51]. used in large commercial or agro-industrial plantations. This review therefore was intended to search the literature Generally, chemical formulations of pesticides are in the on primary/secondary researches on alternatives to form of granules, wettable powders, suspension synthetic pesticides that have potential to manage the concentrates, dustable powders, and aqueous solutions. banana borer weevil. Furthermore, the review points out Most of the chemicals that have been evaluated have limitations for these alternatives and recommends areas contact and/or systemic effects and are usually neurotoxic for future research or that needs improvement. and their effectiveness varies from weak to excellent results. The mode of application of these chemicals are Options for managing Cosmopolites sordidus (i) on the soil around corms, (ii) on corm surfaces, (iii) on pseudostem traps, (iv) in planting holes, (v) planting Like many other important pests on staple crops, lots of materials soaked in insecticide solutions (especially researches have been conducted to provide more emulsive solutions) before planting, and (vi) application at bioecological information on C. sordidus—its structure, life plant collar upto height of 45 cm [4, 10, 41, 55, 66, 67]. In cycle, and population dynamics. Also, with this knowledge, addition, the application rate varies from once to thrice researchers have been testing different techniques that can per year and the dose applied per plant also varies as reduce the population below economic thresholds and follows: (i) for active ingredients it ranges from 0.1 to 2 g, minimize or delay damages caused by the pest. These (ii) for commercial products it ranges from 2 to 100 g or management options that have been evaluated in 1.25 to 50 mL per plant [4, 10, 41, 42]. These variations are laboratories, screen houses, research experimental based on the group of insecticide used, the agroecological stations, and farmers’ farms can be grouped into chemical zones and probably the level of resistance by the weevils. (synthetic and botanicals), microbials (entomopathogens), Of all these classical pesticides evaluated, those with infochemicals, biological control (parasitoids andpredators), excellent efficacies are dieldrin, chlordecone, isophenfos, genetical (resistant varieties, manipulation of cystatins), ethoprophos, terbufos, furadan, aldicarbe, zeta-cypermethrine, physical (trapping), and cultural (sanitation, use of clean imidaclopride, thiametoxam, and fipronil [4, 10, 41–43, planting materials, mulching). While some of these options 61, 64, 68]. However, fipronil and imidacloprid are comprise techniques that have been validated on-farm, relatively new formulations that have been reported some have only shown their potential under controlled with excellent efficacies, having relatively less effect on conditions in laboratories and in screen houses. non-target organisms, and with little or no resistance developed by the weevils [4, 41, 43, 69, 70]. Although these synthetic pesticides have been shown to Use of synthetic pesticides play an important role in modern agriculture and are relatively easier and effective for the management of Many active ingredients from different groups of synthetic C. sordidus, there are reports on the resistance development pesticides have been tested and/or used for the management [4, 26, 61] and on the general adverse effects of pesticides of C. sordidus. The efficiencies of several chemical on human health and on the environment [44, 45, 50, 51, formulations of classical pesticides have been evaluated for 71, 72]. Because of these issues, there has been an

http://www.cabi.org/cabreviews 4 CAB Reviews increasing advocacy for the reduction of these pesticides micro-propagated plantlets are now shifting from their in food production [72, 73] and these have led to the common use of untreated traditional suckers to treated growing concerns and/or tendencies to search for ones or to macro-propagated plantlets. In these small alternatives that could replace them completely or that farms, high proportion of plantains fail to produce due to could be combined with the least toxic chemicals too in an early toppling as a result of root boring nematodes and integrated pest management program. For the case of borer weevils [75]. Disinfected or treated suckers by C. sordidus, commonly evaluated alternatives are use of paring and using hot or boiling water has been shown to infochemicals, entomopathogens, predators/parasitoids, significantly reduce contamination by pathogens and pest botanical pesticides, inhibition by protein enzymes, cultural, [75, 76, 79, 85, 88]. Paring of suckers before planting, paring and genetic techniques. of suckers in combination with sun-drying for 3 days and use of hot water treatment of pared corms before planting have been widely used and shown to have some benefits Alternatives to synthetic pesticides including vigorous growth of the plants, reduced corm damages and root necroses as well as increase in bunch Use of cultural methods weights [76, 88, 89]. Pared and sun-dried plants showed 17% increase in bunch weight [88]. Messiean [26] mentioned Pest management using cultural techniques involves that paring helps to expose larval galleries and therefore manipulation of the environment or implementation of allowing the farmer to reject heavily damaged suckers. preventive practices with the aim to reduce pest population Hot water treatment at 50–55°C of peeled or pared and their damages. Cultural techniques are the oldest suckers for 15–27 min have been reported to significantly methods for managing pest populations although they have reduce weevil and nematode infestations [4, 79, 90–92]. been over shadowed by synthetic pesticides. These However, due to the difficulties in managing and practical techniques are dependent on detailed knowledge of the implementation of this hot water treatment technique, bio-ecological relationships with crop systems. Generally, IITA [93] and Hauser (2010) reported an improved method there have been lots of speculations or hypotheses on the involving immersing pared suckers into boiling water for benefits of these techniques especially to smallholder about 20–30 s. Suckers treated with boiling water produced farmers. Such techniques include mulching, fallowing, crop more bunch than the control [75, 76]. rotation, intercropping, sanitation; cover cropping, trapping, and use of clean planting materials. In this review, we focused on techniques that have been tested in the Fallowing laboratory, screen houses or in the fields. Generally, fallowing involves destroying the crop at a particular piece of land for at least a year before cultivating Clean planting materials again. In the case of bananas and plantains, this practice is very common in large commercial plantations and fallows Using pest and disease-free planting materials (clean are prepared by injecting plants with herbicides before planting materials) is a common technique and has been plowing the field 4[ , 94]. In plantations, after about widely reported to reduce spread of plant parasitic 3–5 years of cultivation, plots are fallowed for about nematodes and different life stages of the banana borer 1–2 years [4, 12]. In some cases, other non-Musa crops weevils [15, 74–83]. InfoMusa [84] also mentioned that a such as sweet potatoes and pineapples are cultivated in combination of several cultural techniques is the best the fallow areas before replanting of bananas/plantains. available approach to resource-poor farmers as it is likely Price [95] recommended at least 1 year of fallowing or to reduce weevil and nematode pressure. The different growing a non-Musa crop before replanting of bananas. clean planting materials are those resulting from tissue Besides suppression of nematodes, some researches have culture (micropropagation), plantlets from corm bits shown limited effects of this practice on the weevils [41, 96]. (macropropagation), and treated traditional suckers. Price [12] showed that weevil damage was lowest According to Viljoen [85], tissue culture plantlets are very (CI = 0.5) in the weed-fallow micro-plots while highest clean since they are produced under sterilized laboratory damage (CI = 2.25) occurred in micro-plots previously conditions and often indexed to ensure they are virus-free. planted with plantains. Based on these results, it was These plantlets are free of soil-borne pathogens and concluded that C. sordidus can cause serious damage to perform well when planted in the field [86]. In spite of young plants planted directly into infested land. New these advantages, only large agro-industrial plantations or plantings nearer to fallows usually have weevils from the large commercial farms mainly use tissue culture plantlets. fallow fields. To make fallows more effective in reducing Although in vitro plants showed vigorous growth and were weevil population and damage to new plantings nearby, taller, they did not show superior performance and higher Rhino et al. [94] introduced the use of pheromones traps yields compared to conventional suckers [87]. Smallholder (9–16 traps per hectare) within banana fallows and farmers who cannot afford and/or have access to these significantly lower catches of adults recorded in new

http://www.cabi.org/cabreviews N.J. Okolle, C. Ngosong, L.T. Nanganoa and L.L. Dopgima 5 plantations adjacent fallows. Also, these catches decreased affect damage to plantain corms by C. sordidus larvae, with the distance from the fallow. Duyck et al. [97] reported although it increased the number of some ant species that 12 months fallow decreases C. sordidus and mass while decreasing others. trapping is effective during the dry season between 40– Banana weevil population has also been found to be 80 days after planting. Mass trapping with pheromones lowest when banana is intercropped with millet while within fallows therefore allows adequate sanitation, yield losses are higher with intercrop and mulch [107– preventing a large part of weevil population leaving fallows 109]. Coffee-banana intercropping was much more and getting into the new plantings, causing damage to the profitable and beneficial than banana monoculture110 [ ]. young plants. The corm damage and yield did not differ between the monoculture and intercrop. The cover crop (Brachiara decumbens) was very useful in providing resources that Use of organic manure/mulching attracted and supported a community of insect herbivores that are alternative prey for potential predators of Mulching is a process of adding a layer of material to the C. sordidus [14]. Poeydebat et al. [111] mentioned that surface of soils during cultivation. Such materials have lower strata species richness had a positive bottom-up demonstrated the ability to protect and improve soil, and effect on herbivore-prey abundance, which in turn therefore enhance crop growth and yields [98–100]. In enhances abundance of predators. Therefore, regulation addition, mulching can play an important role in the of C. sordidus is enhanced through field-scale plant management of pests and diseases [98–102]. Organic and diversification, which increases predators such as ants. inorganic mulches suppressed pests (e.g., , Use of living mulch or intercropping is a common nematodes, and weeds) and diseases (e.g., blight, mosaic practice in developing countries, and it is practiced by viral, and curling diseases). Living/non-living organic many farmers due to declining land sizes and for food mulches have been used to manage pests and diseases on security needs [112]. Musa species and improve their growth and yield. According Non-living mulches are made up of non-living plant to Matkovic et al. [98], living mulches are plants grown in materials that are mostly biodegradable (e.g., straws, saw the field to provide various ecological benefits to the main dust, wood ash, paper, wood chippings, tree backs, grass, crop but are not the main crop. McIntyre et al. showed that plant residues, and composted dung/manure). The leguminuous crops such as Canavalia muzinna and T. vogelli use of such mulches in cropping systems is very common intercropped with bananas repelled borer weevils although as they are cheaper, available, easily acquired, and relatively the yield was unaffected. McIntyre et al. [99] intercropped easy to apply on crops. Unlike living mulches that may some legumes (Canavalia ensiformis, Mucuna pruriens, and compete for resources with the main crop [113], and T. vogelii) with bananas and found out that they did not mainly reduce pest abundance and/or damage on the main affect weevil population or damage as well as fruit yield. crop indirectly (by encouraging the presence of predators The cover crop (Paspalum notatum) reduced adult weevils and parasitoids), non-living mulches do not only encourage but it did not reduce damage to corms while the bunch diversity of beneficial soil-dwelling macro-and micro- weight was significantly lower in cover crop plots than the organisms, but also break down to release nutrients that bare soil, probably due to competition. Gold et al. [103] enhance soil fertility and ultimately crop vigor and yield. reported that weevil populations were higher in mulched Tinzaara et al. [114] used grass mulches (mix of Panicum that unmulched systems, while damage caused varied with maximum, Imperata cylindrica, and Brachiaria spp.) at thin site. They also mentioned that mulching favors growth and (75 kg per plot) and thick (150 kg per plot) levels. Mulching yield but with no advantage for managing C. sordidus. Young had no effect on the number of adult weevils caught in adults were higher in cover crop and negatively correlated pheromone traps and the ratio of male to females captured. with abundance of earwig (Euborellia caraibea) that is an However, more weevils were caught in pheromone traps important generalist predator of C. sordidus in French West in thick mulch plots than the control, especially during the Indies [104]. Salazar et al. [105] intercropped plantains with rainy season. Gold et al. [115] reported that C. sordidus is Mucuna legume cover crop and found that Mucuna more active and move longer distances in mulched than attracted C. sordidus although it did not affect plantain unmulched areas. height, stem diameter, or sucker production when the legume was eliminated 4 months after planting. Dassou et al. [106] showed that using cocoyam, maize and gourd Residue removal (Lagenaria siceraaria) as intercrops for plantains had clear effects on ant abundance, which negatively correlated with These techniques keep the farm or crops clean such that C. sordidus damage for ants of the family Myrmicinae and conditions favoring competitors and pests are minimized positively for Formicine and Ponerinae. Duyck et al. [14] and to allow healthily crop growth. According to Masanza [78], Carval et al. [101] reported that abundance of C. sordidus corms of bananas and plantains are most attractive to and generalist predators such as E. caraibea are affected by weevils than any other crop residues with high oviposition addition of cover crop. Generally, this intercrop did not on freshly harvested residues of up to 30 days. He

http://www.cabi.org/cabreviews 6 CAB Reviews concluded that residues are important source of infestation is only active within a short range and essentially for to standing crops. Okolle and Mbouenda [17] also reported mating purposes and therefore weak as compared to more adult weevils on cut pseudostems, stumps, and sordidine. Generally, pheromones have been used to bunched plants. Although there are many suggestions/ monitor and to mass-trap C. sordidus in attract and kill beliefs on the importance of residue removal, weeding, and programs. Pheromone-bated pitfall traps are commonly pruning for managing C. sordidus, very little research used and are very effective in reducing adult weevil population (supported with data) has been carried out on this. In his compared to all the variants of pseudostem traps and field experiment, Masanza 78[ ] showed that removal and other pheromone-baited traps [4, 118, 120, 125, 129]. To chopping of crop residues in farmers’ fields helped to keep retain adult weevils that fall into the trap, water containing C. sordidus populations and damage lower than when 1–3% dish washing detergent is placed in the traps. A major residues were left to accumulate, leading to a 34% setback for pheromone-baited pitfall is that they are easily reduction in yields. However, he reported that complete flooded during the rainy season, very expensive and not removal of residues lead to significant reduction in affordable or easily accessible for smallholders. In South natural enemies compared to leaving residues. Africa, De Graaf [41] reported that there were no significant Inzaule et al. [116] reported that experimental plots differences between normal pseudostem traps and the with cultural practices such as desuckering, detrashing, control (pit fall traps without baits or lures) with over chopping of pseudostems decreased weevil, and nematode 65.3% female weevils caught. The efficacy of pheromone- damage. baited traps is enhanced when they are integrated with some plant parts. Tinzaara et al. [130] reported that C. sordidus responded significantly stronger to the Trapping combination of synthetic pheromone and fermented pseudostem (AAA-EA) than to pheromone or pseudostem Trapping is a physical technique intended to exclude a pest alone. Osorio et al. [121] found that with the exception of such that it does not reach the target and cause damage. corms, there were no statistical differences between Generally, traps are used to catch and either destroy or pheromone traps mixed with other plantain parts and poison adult weevils. An old trapping method in research pheromones alone, while pheromone traps mixed with stations and most farms is the use of classical split corms captured more weevils. In Ghana, Jallow et al. [120] pseudostems [15, 26, 95, 108, 117]. Classical pseudostem did not find any significant differences between corm and traps are usually about 30 cm in length and cut from pseudostem traps, although the corm traps caught more harvested pseudostem stumps or pseudostem residues on weevils. Dead banana leaves have also been found to be the soil. Although at present it is difficult for most farmers more attractive to weevils than pseudostem and rhizome (small-scale) to adopt this technique, most plantations materials [131, 132]. (large-scale) adopted it but soon abandoned it because it is labor-intensive, costly and time wasting [118]. Other traps called disc-on-corm traps [4] have been made from Use of plants with insecticidal properties corms of harvested stumps by cutting out a small pieces of corms from harvested stumps, removing it and placing it Plants with bioactive properties are also referred to as again on the cut spot such that an allowance is left for botanical pesticides or they can be categorized as weevil entry. Similarly, Ogenga-Latigo and Bakyalire [119] biorational pesticides [4, 133]. Generally, these type of described a disc-on-stump trap made by cutting harvested pesticides should have low toxicity to non-target organisms stump 15–25 cm above-ground level and placing a 5–10 cm and suppress pest populations by affecting their orientation thick pseudostem disc on top of the stump. Although disc- and reproductive behaviour. In addition, these botanical on-corm and disc-on-stump catch more weevils than the pesticides also pose little threat to the environment and classical split pseudostem traps, they are still labor- human health [134]. Although many smallholder farmers intensive, relatively difficult to set, and are inflexible. To commonly and quickly adopt synthetic pesticides for the overcome this problem, many researchers and large-scale management of pests, plants with insecticidal properties plantations are now using pheromones as lure for banana have been used and are now gaining more support as more borer weevils [54, 120–125]. Sordidine is a male-produced evidences arise on the threats of synthetic pesticides aggregation pheromone isolated from banana borer on the environment and human health. Table 1 below weevils and was identified by Beauhaire et al. [126]. This shows 31 different plant species from 15 Families have pheromone is commonly sold in commercial packs with been evaluated for the management of C. sordidus, with trade names such as Cosmolure®, CosmoPlus®, and many of the experiments conducted in the laboratory. Of Cosmotrak®, and Budenberg et al. [127] first provided these plant Families, the most frequently evaluated have evidence for this pheromone. been Solanaceae, Asteraceae, and Meliaceae. However, In addition to sordidine, Uzakah et al. [128] provided commercial products for the management of C. sordidus evidence for the presence of a female produced sex have been developed mainly from Meliaceae (e.g., neem pheromone. However, they mentioned that this pheromone plant) and Solanaceae (e.g., chili pepper).

http://www.cabi.org/cabreviews N.J. Okolle, C. Ngosong, L.T. Nanganoa and L.L. Dopgima 7 Continued C. sordidus No significant differences in fields where synthetic pesticides and ethnomedicinal plant extracts were used. Feeding deterrence for larvae. Surviving larvae with significantly smaller sizes and weight. Repulsive to weevils. Significantly reduced the total haemocyte counts for weevils. Oviposition significantly low on corms treated with the plant extracts. Limited toxicity on adults (only 5.5% mortality). Repellent properties also limited. Oviposition significantly reduced. Good repellents although very weak for ash. Effects on • • • Larval mortality. • • Oviposition deterrence. • • 6.7% mortality. • • • • • form, cake and oil. product—Neem Gold® Parts used Not mentioned Not mentioned Not mentioned Not mentioned Not mentioned Not mentioned Seed in powder Commercial Ripe seeds Leaves Leaves Leaves Leaves Fruits/seeds . Family Solanaceae Solanaceae Phytolaccaceae Asteraceae Fabaceae Asteraceae Meliaceae Meliaceae Meliaceae Asteraceae Pontederiaceae Euphorbiaceae Solanaceae Solanaceae C. sordidus cayenne pepper; tabasco pepper India, Bead-tree, Cape lilac, Common name Chili pepper, bird pepper; Tobacco African soapberry Wild sunflower Fish poison bean Fireweed, Okinawa Spinach Neem Neem Chinaberry tree, Pride of Syringa berrytree, Persian lilac, Indian lilac, Mexican marigold Water hyacinth Castor oil Tobacco Pepper spp. spp. spp. Plants evaluated Capsicum frutencesis Nicotiana Phytolaca dodecandra diversifolia Tithonia vogelii Tephrosia Crassocephalum crepidiodes Azadirachta indica Azadirachta indica Melia azedarach Tagates Eichornia crassipes Ricinus communis Nicotiana tabacum Capsicum ] 136 ] ] . [ ] 133 124 et al . [ . [ 135 . [ Different plant species screened and tested for their potential to manage et al et al

et al ] 137 [ Table 1. Table References Bwogi Musabyimana Sahayaraj and Kombiah Tinzaara Tinzaara

http://www.cabi.org/cabreviews 8 CAB Reviews S. - and Piper guineense elicited repellence of class C. sordidus powder and solution caused reduces oviposition on corm P. nigrum P. 100% mortality and over 90% repulsion. nigrum P. surface by 50%. All extracts showed repellent effects which were dose-dependent. aromaticum IV (60.1–80%). Very poor repellence and mortality for weevils but higher efficacy for mealy bugs (73.3% compared to 53.3% for Fipronil). All the plant parts for fresh and dry crude extracts caused high mortality (>70%) for eggs and larvae. Had significant deterrence and repel lence effects on adults. Significantly affected oviposition on treated corms (less eggs laid). Effects on • • • • However, only • • • • of a commercial product Bromorex® material material Parts used Seeds Seeds Leaves Seeds Leaves Seeds Seeds Seeds Leaves Seeds Fruits Fruits Stems Extracts in the form Whole plant Whole plant Gluttiferae or Fabaceae or Mimocaceae Family Piperaceae Zingiberaceae Amaryllidaceae Meliaceae Poaceae Annonaceae Clusiaceae or Annonaceae Lamiaceae Piperaceae Leguminosae Myrtaceae Zingiberaceae Solanaceae Asteraceae Phytolaccaceae alligator pepper respectively. pepper, false cubeb, Guinea cubeb Pokeberry, Pokeroot, Poke sallet, and Ink berry Common name Black bush pepper Grains of paradise or Onion and Garlic, Neem Lemon grass English pepper fruit Bitter cola Calabash nutmeg Clove basil or African Ashanti pepper, Benin Aidan tree The clove tree Ginger Chili pepper Wild sunflower Pokeweeds, Pokebush, Allium and spp. sativum Plants evaluated Piper nigrum Aframomum melegueta Allium cepa Azadirachta indica Cymbopogon citratus Dennetia tripetala Garcinia kola Mondora myristica Ocimum gratissimum Piper guineense tetraptera Tetrapleura Syzygium aromaticum Zingiber officinale Capsicum annuum diversifolia Tithonia Phytolacca ] 139 ] . [ 69 et al Continued. ] 138 [ Table 1. Table References Debonnaire [ Inyang and Emosairue Manka and Okolle [70] Mukassa

http://www.cabi.org/cabreviews N.J. Okolle, C. Ngosong, L.T. Nanganoa and L.L. Dopgima 9 With the exception of Piper spp. with very high is increasing interest of EPFs for controlling root-feeding mortality on adult weevils, most evaluated plants had pests [143, 144]. The common commercially available little or no direct toxicity on adult weevils. In one study, EPF-based products to control root pests include three neem caused mortality of larvae while T. diversifolia and genera of opportunistic insect pathogens: Beauveria or Phytolacca spp. caused high mortality to eggs and larvae. Cordyceps [145] (Hypocreales: Cordycipitaceae), Metharizium However, most of the plant extracts showed significant (Hypocreales: Clavicipitaceae), and Isaria (Hypocreales: indirect or non-mortality effects such as repellency, Cordycipitaceae). Delattre and Jean-Bart [146] were the oviposition deterrence, feeding deterrence, significant first to evaluate different strains of entomopathogenic reduction in weight and size of larvae, as well as a case fungi on C. sordidus. Of the several researches conducted, that resulted to reduced number of haemocytes in adult many have tested the potential of EPFs to manage d weevils. Most experimental screening and testing of these C. sordidus in the laboratory [147–156] and field [152, 153, plants with bioactive properties have been conducted in 157–161]. the laboratory (with few field tests) and we could not Although different results were obtained based on the find any that tested the effects of botanicals on non- strains of B. bassiana and M. anisopliae used, concentration, target beneficial organisms within banana agroecosystems. method of application or delivery of the fungi, integration An important finding from Messiaen 26[ ] is that the with other management options, environmental conditions collection site of neem plants affects its effectiveness, and and even length of storage, B. bassiana has shown strong those from North Cameroon were better than those potential to manage C. sordidus. Table 2 shows some tested from South Cameroon. isolates, concentrations, and their effects on C. sordidus. With particular interest on the high potential of enhancing efficacy of entomopathogens by using conventional host Use of pathogens, predators, and parasitoids plant traps and pheromone traps [152, 156, 161]. Compared to pseudostem traps, incision traps on corms The use of living organisms (microscopic or macroscopic) attract more weevils and therefore when treated with B. and/or their products to manage pests is referred to as bassiana, caused higher mortality. Generally, indigenous biological control. Of particular importance is the use of strains are more pathogenic to adult weevils [149, 152, parasitoids, pathogens, predators, antagonists, or competitors 164] and those on insect body are more persistent than to suppress pest population, making their population less those on substrates. Commonly used substrates are abundant and less damaging than it will be in the absence bagase rice, bagase beans, maize grains, soil, vegetable oil, of biocontrol agent [140]. For C. sordidus management, although higher efficacy was recorded on maize and soil most researches have focused on entomopathogens and formulations. An inportant factor that makes B. bassiana an predators. effective biological control agent for C. sordidus is that infected living adult weevils can spread and transmit the infection to other healthy weevils. In the laboratory, Entomopathogenic organisms Omukoko [155] recorded 24–26% mortality of weevils as a result of such transmission of infection. According to Entomopathogens or microbial agents that have been Fancelli et al. [148], several factors account for variation of tested against C. sordidus include entomopathogenic fungi effectiveness of B. bassiana in the field, such as strain, such as Beauveria bassiana and Metarhizium anisopliae, variety of crop, climate, and method of application of entomopathogenic nematodes such as Steinernema spp. fungus. In addition to traps, B. bassiana can be integrated and Heterorhabditis spp. and endophytes such as non- with pesticides. Sirjusingh et al. [159] reported that pathogenic Fusarium spp. Entomopathogenic fungi and reduced doses of pesticides combined with fungal spores nematodes are mostly used to kill adult weevils, while resulted in higher mortality of adult weevils but not a endophytes effectively control the immature stages of better development of mycosis a synergistic effect. the pest. Entomopathogens reportedly established Similarly, Okolle and Lombi showed that combination of following applications in banana fields in some cases but imidacloprid and commercial B. bassiana (Botanigard®) without adequate establishment, entomopathogens reduced weevil damage in the field. would require repeated applications as a biopesticide Besides the direct use of B. bassiana as biopesticide, these and this entails continued production, distribution, and entomopathogenic fungi and other non-pathogenic fungi storage costs. provide bioprotection services to banana and plantain plants. By performing this role, they are referred to as endophytes— microscopic organisms that colonize plant tissues internally Entomopathogenic fungi andendophytes for at least part of their life cycle to form mutualistic Studies exploring the potential of entomopathogenic fungi relationships with their host plants including antagonism (EPF) in biocontrol indicate a striking asymmetry between to pests and diseases. According to Tixier et al. [165], above- and below-ground target pests. While, studies on bioprotection of banana vitro plants with endophytic fungi EPFs have focused on above-ground pests [141, 142], there such as non-pathogenic Fusarium oxysporium is an innovative

http://www.cabi.org/cabreviews 10 CAB Reviews Table 2. Different entomopathogenic fungi isolates evaluated for the management of C. sordidus, their concentration, and major results obtained.

Fungal isolate/strain Concentration used Key results Reference B. bassiana (G41) 3.4 × 1011spores/mL (in Significantly more pathogenic to the adult weevils [152] (indigenous) the laboratory) than foreign isolates 1.25 × 108 spores/mL (in Reduced hatchability of eggs pot experiment) 3.54 × 1012 spores/mL in Significantly reduced weevil population and damage the field applied on top and persistent on soil soil around plants B. bassiana (CG1013) 2.6 × 108 spores/mL (in Caused mortality of 90–93.7% to adult weevils [162] the laboratory) B. bassiana 3.1–3.2 × 109 conidia/g Caused adult weevil mortality of 80% in 30 days and [163] cultured on cracked a 20% drop in mortality after 180 days in storage maize grains (in the laboratory) 6 Cordyceps bassiana LC50 of 6.4 × 10 and In the laboratory: Caused adult mortality of [145] (Cb171, Cb190, 5.4 × 106 conidia/mL 77.5–80.2%. Cb174) (in the laboratory Reduced weevil population by 48.5% and with over and field) at LT50 of 50% mycosis of trapped weevils in the field 9.49–9.55 days 6 M. anisopliae (Ma148) LC50 of 8.6 × 10 conidia Virulent and causing 76.9% adult mortality in the per mL at LT50 of laboratory. 12.6 days Reduced weevil population by 48.5% with over 50% mycosis of trapped weevils in the field B. bassiana (G41) 3 × 109 conidia/g in the Weevils captured from plots where conventional [156] lab and on-station field traps were treated with G41 showed significantly higher percent mycosis (25.9%) compared to those where the fungus was applied around banana mats B. bassiana (ICIPE 237, 108, 3 × 108, 109 in the Pathogenic to adult weevils although virulence was [154] M353, M207) laboratory significantly different with different concentrations. ICIPE 237 as the most virulent at LC50 of 4.22– 8.89 × 108 conidia/mL and LT50 of 31–51 days B. bassiana (ICIPE 273, 1 × 108 in the laboratory All were pathogenic although ICIPE 273 was the [155] ICIPE 645, ICIPE 281) best causing weevil mortality of 50–70% in 40 days B. bassiana (CNPMF 1 × 108 in the laboratory In the laboratory, these isolates caused about 96% [148] 407, CNPMF 218, and then in the field mortality. In the field, CNMPF 218 was most CNMPF 416) efficient causing about 20% mortality leading to 40% reduction in weevil population size after 12 months

option for controlling C. sordidus. The role of different Metarhizum spp. and Beauveria spp. have evolved as isolates of non-pathogenic fungi as endophytes that can characteristic root endophytes [142, 169, 172–174], manage banana borer weevils have been studied [166– facilitating nutrient absorption, and offering substantial 168]. Dubois et al. [169] evaluated 15 strains of Fusarium protection against tunneling insect pests. In a screen spp. isolated from corms and roots of banana plants. The house experiment, 15 days after weevil infestation and endophytes from roots that were inoculated into plants endophyte of plants, Akello et al. [175] recorded 53.4– caused higher mortalities (up to 50%) of C. sordidus eggs 57.7% mortality of adult weevils as a result of B. bassiana with strains V2w2 and V5w2 as the best. In the field, infection resulting in reduction of plant damage by 29.1– Ochieno [170] showed that C. sordidus has low preference 62.7%. They also reported that this endophyte can for plants inoculated with two endophytes—F. oxysporum colonize tissue cultured plants for at least 4 months after V5w2 and B. bassiana G41 while corm damage was low for inoculation. In addition, in a screen house experiment, F. oxysporum V5w2-treated plants. Paparu et al. [171] Akello et al. [176] at inoculation rate of 1.5 × 107 conidia/ showed that isolates of F. oxysporum served as endophytes mL for 2 h and 2 weeks after larval infestation, reported with root colonization highest in inoculated plants, with that B. bassiana endophyte significantly reduced larval better colonization and significant weevil damage for survivorship (23.5–88.9% mycosis) resulting in 42–86.7% V5w2 isolate. In addition to their pathogenicity, some reduction of plant damage.

http://www.cabi.org/cabreviews N.J. Okolle, C. Ngosong, L.T. Nanganoa and L.L. Dopgima 11 Entomopathogenic nematodes Furthermore, weevil larvae were more susceptible to Among the most promising biocontrol agents of root pests isolates of Heterorhabditidae family. Mwaniki [198] are the soil-borne entomopathogenic nematodes (EPNs) reported that the local EPNs isolated do not infect adult in the families Steinernematidae and Heterorhabditidae weevils and therefore no mortality was observed. Although that are obligate parasites of [177–180]. The the entire test EPNs caused more than 90% mortality for third juvenile stage is the “infective juvenile” that is free- weevil larvae, S. carpocapsae was the most virulent at 300, living in soil and used in biocontrol [181, 182]. 400, and 500 IJ/larva. In a commercial banana plantation, Entomopathogenic nematodes are soil-dwelling and Schmitt et al. [199] applied dose of 5 × 106 IJ/m2 onto split naturally occurring organisms but they can be isolated pseudostems and pseudostem stumps as a baiting from soils and produced commercially [183, 184]. EPNs technique and recorded 70% mortality of adult C. sordidus have received attention as biocontrol agents because of recovered from the traps 7 days after treatment. Application their wide host range, ability to kill host rapidly, can of EPN to pseudostem traps resulted to significantly easily be mass produced and applied, and long-term greater control of weevils than application on the soil efficacy with no adverse effect on the environment [185, around banana. 186]. Generally, once EPN infective juveniles get into an insect’s hemolymph, it releases highly specialized symbiotic Entomopathogenic bacteria and viruses bacterium (Xenorhabdus spp.) found only in EPNs. The We found only two researches that evaluated the effect of bacterium multiplies rapidly to kill the insect, making entomopathogenic bacteria. Kaya et al. [151] found that the cadaver more suitable for nematodes to feed on. the entomopathogenic bacteria Serratia marcescens caused Most studies on the use of EPNs to manage banana mortality of third instars of C. sordidus at LT50 of 2.8 days borer weevils are laboratory based with few in the field. although it did not kill adults even at 10 times the Laboratory trials demonstrated susceptibility of adult C. concentration applied for larvae. About 0.24 ppm for sordidus to Neoaplectana carpocapsae [187, 188] while Bacillus thuringiensis crystal (CRY6A) toxins resulted in 50% Figueroa [189], mentioned the genus Steinemema as a mortality (LD50) of neonate larvae [200]. potential biocontrol agent for C. sordidus. These nematodes have demonstrated efficacy to destroy a wide range of soil-borne and stem-boring insects that attack agricultural Predators and parasitoids crops [190–192]. Treverrow and Bedding [193] developed a delivery system that involved releasing nematodes into Banana and plantain farms usually have microenvironments conical shaped cuts made in residual rhizomes that developed that favor the survival of a complex of natural enemies mutualistic relationships with plants, and act as antagonists especially predators. These microenvironments include to pests and diseases. Although these nematodes reduced residues (harvested pseudostem stumps, cut pseudostems, weevil numbers, they were not economically competitive pruned leaves, and patches of weeds), parts of living plants with pesticides [194]. Bortoluzzi et al. [195] tested the (within old leaf sheaths), and drainage channels in the case pathogenicity of different isolates of EPNs (at 100 infective of large commercial plantations. Most of these areas have juvenile (IJ)/cm2 applied on cut pseudostem placed in also been reported as most preferred sites/habitats of plastic containers in the laboratory) from the families C. sordidus [201]. Several researches were conducted to Heterorhabaditidae and Steinernematidae. They recorded search for indigenous and exotic predators and parasitoids, variations in mortality (0–36.7% within 2–7 days) of adult as well as testing their abilities to manage borer weevils C. sordidus with highest mortality from Heterorhabditis spp. under laboratory and field conditions 37[ , 106, 201–209]. isolate IBCBn40. Combination of EPNs with insecticide Many of these have resulted to a listing of potential (carbofuran) did not affect viability of IJ, although it caused predators/parasitoids and few studies actually tested the reduction in infectivity. impact of these predators/parasitoids for managing the pest. In another laboratory experiment, Amador et al. [196] Table 3 lists different potential predators of C. sordidus, of evaluated the susceptibility of C. sordidus adults and larvae which most are Coleopterans (), Hymenopterans to H. atacamensis isolate CIA-NEO7. No mortality on (ants), and Dermapterans (earwigs). A case has also been adult weevils while different concentrations of 100, 500, mentioned of a vertebrate (the cane toad) that eats adults and 1000 IJ per larva were significantly different from the of C. sordidus [210] while upon dissection of toads collected control and resulted to LD50 of 52 IJ/larva. When larvae from the fields in Martinque, Okolle 4[ ] also recovered were in the corm, LD50 increased to 375 IJ/larva and weevil dead weevils from their stomachs. larvae within banana corms infected with EPN had 80% As far as parasitoids are concerned, attempts to rear mortality 10 days after inoculation at 1000 IJ/larva. Kutnjem them from C. sordidus life stages have all been negative. et al. [197] tested local isolates of Heterorhabditis and Traore [211] tried to use carrot weevils (Listronotus Steinernema and showed that mortality of C. sordidus adults oregonensis and L. texanus) parasitoid (Anaphes sordidatus) of the different isolates ranged from 3 to 40% after 12 days but failed. The parasitoids laid eggs into eggs of C. sordidus after treatment while that for C. sordidus larvae was 84% at but no emergence of larvae or adult parasitoids were concentration of 40 IJ/larva 2 days after treatment. recorded. After thorough field searches, Tinzaara and

http://www.cabi.org/cabreviews 12 CAB Reviews Table 3. List of potential predators of the banana borer weevil (C. sordidus).

Predator Order (Family) Observations Reference Plasius javanus Coleoptera (Histeridae) Usually found within mats and Abera-Kalibata et al. [204] Plasius laevigatus residues. Hololepta spp. For the non-social predators, Belonochus ferrugatus Coleoptera (Staphylinidae) Dermaptera was most abundant. Leptochirus unicolor Coleoptera (Staphylinidae) Among ant species, the Formicinae, Earwigs Dermaptera (Forfuculidae, Ponerinae, and Myrmicinae were Labiidae, Chelisochidae) most widely distributed and Ants Hymenoptera—Formicidae abundant. (Ponerinae, Formicinae, Chelisochidae consumed more of Ponerinae, Amblyoponinae, C.sordidus eggs while larvae and Formicinae, Myrmicinae, adults of P. javanus consumed much Dolichoderinae) of larvae and pupae of the pest Pheidole spp. Hymenoptera—Formicidae In the laboratory, eggs, larvae and Abera-Kalibata et al. [202] (Myrmicinae) pupae of the pest reduced by ants Odontomachus Hymenoptera—Formicidae only at low densities. troglodytes (Formicinae) In the field, at full crop cycle, ants reduced densities of the weevil eggs only. Ants Hymenoptera—Formicidae Pheidole spp., Lepisiota spp & Abera-Kalibata et al. [203] (Dorylinae, Dolichoderinae, Paratrechina spp. were most Formicinae, Myrmicinae, abundant in the field. Ponerinae) O. troglodytes and Pheidole spp. were most significant in consuming the pest immature life stages in plants and residues. These ants could remove 33–68% eggs from naturally infested corms P. javanus (Histeridae) The ant species Myopopone casta- Hasyim et al. [207] Earwigs Dermaptera (Chelisochidae) nea (Ponerinae) seen attacking the Ants Hymenoptera—Formicidae weevil larvae in crop residues in the (Dolichoderinae, Formicinae, field. Myrmicinae, Ponerinae) P. javanus larvae and adults were best in consuming the pest larvae and pupae (53–87% while the Chelisodid earwig was the best for eggs (42%) Eutachia pulla Coleoptera (Tenebrionidae) These predators reduced weevil eggs Koppenhofer [37] Euborellia annulipes Dermaptera (Anisolabidae or population in the field at a rate of Caroinophoridae) between 20.5–44% Dactylosternum Coleoptera (Hydrophilidae) abdominal Pheidole Hymenoptera—Formicidae P. megacephala and T. guineense Castineiras et al. [206] megacephala (Myrmicinae) had best results in the field. Tetramorium Hymenoptera—Formicidae P. megacephala caused 55% guineense. (Myrmicinae) reduction of weevil population and Azteca spp. Hymenoptera—Formicidae 65% reduction in corm damage. (Dolichoderinae) T. guineense causes 83% mortality of Solenopsis geminata Hymenoptera—Formicidae weevil larvae in low infested fields (Myrmicinae) and 67% in highly infested fields Wasmannia Hymenoptera—Formicidae auropunctata (Myrmicinae) Pheidole fallax Hymenoptera—Formicidae (Myrmicinae) Continued

http://www.cabi.org/cabreviews N.J. Okolle, C. Ngosong, L.T. Nanganoa and L.L. Dopgima 13 Table 3. Continued.

Predator Order (Family) Observations Reference Axinidris spp. Hymenoptera—Formicidae Intercropping banana with maize had Dassou et al. [106] (Dolichoderinae) clear effects on ant abundance, Camponotus spp. Hymenoptera—Formicidae which was negatively correlated with (Formicinae) C. sordidus damage for Myrmicinae Odontomachus mayi Hymenoptera—Formicidae and positively correlated for (Myrmicinae) Formicinae Paratrechina Hymenoptera—Formicidae longicornis (Formicinae) Pheidole spp. Hymenoptera—Formicidae Tetramorium spp. (Myrmicinae) Odontomachus spp. Hymenoptera—Formicidae Most common predators were Tinzaara and Karamura (Formicinae) Odontomachus and Dactylosternum. [18] Dactylosternum spp. Coleoptera (Hydrophilidae) Euborellia, Labia and Thyreceophalus Euborellia spp. Dermaptera (Anisolabididae) were most promising as they Odontomachus spp. Hymenoptera—Formicidae consume more eggs, larvae and (Formicinae) pupae Labia spp. Dermaptera (Spongiphoridae) Labia spp. had highest searchability Thyreceophalus spp. Coleoptera (Staphilinidae) based on consumption of hidden eggs in the laboratory Bufo marinus—Cane Anura (Bufonidae) Feeds on the weevil in the field Pinese et al. [210] toad Dactylosternum Coleoptera (Hydrophilidae) These generalist predators used Tinzaara et al. [209] abdominal volatiles from fermented banana Pheidole Hymenoptera—Formicidae pseudostem tissues as the major megacephala (Myrmicinae) chemical cue when searching for Euborella annulipes Dermaptera (Anisolabididae) prey Thyreocephalus Coleoptera (Staphilinidae) interocularis

Karamura [18] did not find any parasitoids of the pest and cultivars that are resistant to pest through identification of no parasitism for C. sordidus eggs, larvae, and pupae. resistant cultivars, resistance mechanisms, crossing, and Koppenhofer [212] did not also find any parasitoids from all possibilities of engineering genes that are deleterious to the indigenous natural enemies recorded, which is probably weevils ([16, 214–231]. due to the cryptic nature of weevils (the larvae and pupae hiding and found deep into pseudostem or corm). In Indonesia (one of the native places of the weevils), Hasyim Screening for resistant varieties et al. [213] obtained phorid parasitoids from both larvae and pupae of C. sordidus although parasitism was very low. Kiggundu et al. [231] highlighted the importance of identifying Abera-Kalibata et al. [204] and Hasyim et al. [207] not only resistance and its incorporation into breeding programs reported no parasitism of weevil eggs and larvae, but also for improving the available germplasm. Generally, field recovered phorids (Megaselia spp.) and drosophilids from screenings using damage scores resulting from weevil larval rearings, which most likely were scavengers. attacks are used to identify resistant or susceptible cultivars. Although plantains and East African Highland bananas have been found to be more susceptible to weevils, Resistant varieties and genetic modification there are some exceptions and variations. In India, two plantain cultivars (Karumpoovan and Poozhachendou) and According to Seshu-Reddy and Lubega [214] and Haubruge in Cameroon the plantain Kedong Kekang were found to and Amichot [46] host-plant resistance is a potential long- be resistant [216, 232]. Table 4 shows the response of term intervention to control banana borer weevils on different genomic groups to banana borer weevil. Ocan small-scale farms within an integrated pest management et al. [225] reported that genotypes with “B” genome are perspective. Although the use of synthetic pesticides is more tolerant to banana weevils than genotypes with usually effective, most pesticides easily become ineffective only “A” genomes, while Mesquita et al. [240] mentioned due to the quick development of resistance by the weevils that AA genome progenitor M. acuminata is more or insects in general [4, 61, 215]. Several researches have susceptible to weevils than BB progenitor M. Balbissiana. therefore focused on breeding programs that develop Many hybrids have been reported display high levels of

http://www.cabi.org/cabreviews 14 CAB Reviews Table 4. Different Musa genomic group response to search, locate and oviposition on both susceptible and banana borer weevils. resistant varieties and there was no significant difference on egg laying on/into the varieties [127, 218, 220, 226, 239, Genomic 242]. Rwekika [220] found that salicin (a phenolic glucoside) response Reference Country and glucose were significant feeding attractants to banana AAB Haddad et al. [233] Venezuela weevils with higher levels found in susceptible cultivars as Susceptible Seshu-Reddy and Lubega [214] Kenya compared to the resistant ones. Similarly, Ndiege et al. Speijer et al. [234] Kenya [243] identified another chemical (1,8-cineole) as the active Gold et al. [235] Uganda component of volatiles released from some susceptible Fogain and Price [216] Cameroon varieties. Results from laboratory studies have shown that Musabyimana [236] Kenya the main mechanism for resistance of Musa spp. to the Kiggundu et al. [231] Uganda Teixeira de Oliveira [227] Brazil pest is antibiosis [17, 217, 231, 239]. In these studies, egg/ AAB Irizarry et al. [237] Pueto Rico larval mortality was lowest on resistant varieties and Resistant Kiggundu et al. [231] Uganda highest on susceptible ones. In some, the developmental ABB Viswanath [238] India cycle from ovipostion to adult emergence is lengthened in Susceptible resistant varieties. Corm hardness and latex quantity/ ABB Seshu-Reddy and Lubega [214] Kenya viscosity were reported to have negative effect on egg Resistant Speijer et al. [234] Kenya hatchability and survivorship of first intars 231[ ]. Gold et al. [235] Uganda Ortiz et al. [218] Nigeria Musabyimana [236] Kenya Engineering of chemicals deleterious to the weevils Abera [239] Uganda Rwekika [220] Tanzania Kiggundu et al. [231] Uganda There exist genetically modified Musa species but the use and acceptability or adoption of these transgenics has been Source: Kiggundu et al. [231] with additions and light modifications very controversial especially for biosafety concerns and by the present authors these are usually resistant to different diseases and nematodes that attack bananas and plantains but not C. sordidus. resistance [222, 226, 227, 231], but few were susceptible. However, researches have identified and tested the toxicity Some varieties reported with high resistance to the of phytocystatins on banana borer weevil larvae [200, 223, weevil are Yangambi Km5 (AAA), Sanna Chenkadali, 224, 228, 244]. These researches showed natural Sakkah, Senkadali, Elacazha, Njalipoovan, Pisang Awak susceptibility of C. sordidus to some identified phytocystatins. (ABB), Kivuvu (ABB), FHIA 03, TMBx612-74, TMBx6142-1, Phytocystatins are proteinaceous inhibitors of plant origin TMB2x8075-7, Long Tavoy, Njeru, Muraru, Calcutta-4 that inhibit specifically cysteine proteases by forming tight (AA-wild type), Bluggoe, M. balbissiana, Cavendish (AAA), irreversible bonds, thus preventing the hydrolysis of proteins Gros Michel (AAA), Kayinja (ABB), Ndiizi (AAB), Kisubi by proteases. According to Kiggundu [224], cysteine (AB), FHIA-03 (AABB), Nalikira (AAA-EA), Prata Ana protease inhibitors (cystatins) are expressed in response to (AAB), Pacovan (AAB), M3, M4, M5, M6, M8, CRBP-60, wounding and insect herbivory and they form part of the CRBP-39, CRBP-969, Karumpoovan, Poozhachendu, native host plant defense system. Cysteine proteases are Kedong Kekang [4, 215, 216, 222, 226, 227, 231, 241]. enzymes usually found in the mid-gut of coleopteran insects such as C. sordidus with an important role of breaking down dietary proteins. Any substance that inhibits the functioning Resistance mechanisms of proteases has direct effect on protein digestion of the Kiggundu et al. [231] described three possible resistance insect, resulting in protein deficiency and affecting insect mechanisms in insect-host plant relationships: development and survival. i. Non-preference or antixenosis—ability to locate and Montesdeoca et al. [244] found that neonate larvae of accept to feed or oviposit on a particular plant. C. sordidus fed on diets containing 0.2% (w/w) of soybean ii. Antibiosis—adverse, usually biological effects to the Kunitz trypsin inhibitor (STI) experienced lower survival insect trying to utilize a plant species. rates and displayed significant reduction in growth. Larvae iii. Tolerance—a variety being able to survive a pest reared on this STI diet also had reduced trypsin activity. population that would otherwise be destructive to another Kiggundu [224] reported that phytocystatins resulted to susceptible variety. 60% reduction in body weight of young larvae and Mesquita [240] found that banana weevil preferred reduction in growth rate. Elyeza [200] showed that 50% particular cultivars for feeding and oviposition, and that mortality (LD50) of neonate larvae was observed at susceptibility of Musa spp. varies both between and within 0.24 ppm and 0.15 ppm for Bacillus thuringiensis crystal genomic groups. In most studies, there was no case that (CRY6A) and Carica papaya cystatin (CPCYS) toxins, supported antixenosis as the main resistance mechanism respectively. This research also resulted in a modified for C. sordidus because weevils were found to be able to artificial diet that could sustain 70% of C. sordidus as well as

http://www.cabi.org/cabreviews N.J. Okolle, C. Ngosong, L.T. Nanganoa and L.L. Dopgima 15 using the diet to establish efficacy of these recombinant effects of different clean planting materials on C. sordidus proteins, which is a basis for developing transgenic bananas damage and yield of Musa spp. under field conditions. with improved resistance against borer weevil. • Fallowing and rotation are other common practices with large commercial or agro-industrial plantations, but land scarcity also highlight the need for more research Conclusions, gaps/limitations, and to ascertain the impact on bananas and plantains. recommendations for further research • Cover crops such as Mucuna spp. and Brachiara decum- bens provide useful ecosystem service that attracts Generally, banana or plantain corm borer weevil (C. sordidus) hervivorous insects and generalist predators, but de- is the most reported economically important insect pest tailed studies are necessary to provide insights into on Musa species. the impact of such mulches on weevil population dy- namics, corm damage, plant growth, and yield. • Trapping is an old method with small-scale farmers eas- Use of synthetic pesticides ily applying the classical split pseudostem traps while large commercial farms are vest with pheromone traps. • It is the oldest method for C. sordidus control/manage- • Pheromone-baited traps are very effective in captur- ment and many different active ingredients have been ing adult banana borer weevils and are very compati- used with varying results (moderate to excellent). ble. However, the effectiveness varies with several fac- • C. sordidus has been reported in most areas that Musa tors such as exposure to sunlight, relative humidity, species are grown and it is commonly managed using temperature, season (wet or dry), irrigation, farm site, synthetic pesticides (mainly of organophosphorus, rainfall, trap size, trap type (ramp or pitfall), trap color carbamate, phenylpyrazole, and neonicotinoid groups). (white, brown, mahogany brown, black, yellow) dura- • Pesticides that are normally not registered for use in tion of trapping, trapping material, pheromone release banana or plantain farms are often misused. rate, release distance, trap location, and farm manage- • There is a need to periodically assess common pest ment practices [122]. The number of traps per hectare management practices performed by farmers, espe- depends on the purpose (detection, monitoring, or cially in developing countries. In addition, detailed stud- mass trapping). Range of 4–25 traps per hectare has ies are required to elucidate on the effects of pesti- been used with a maximum mean trap catch per day cides on non-target beneficial organisms within Musa of about 60 weevils. Research results also showed spp. agroecosystems. variations between the number of weevils caught in • In spite of their effectiveness, weevils develop resistance traps and the damage on plants. Despite the effective- to these pesticides, which leads to ecological backlash ness and compatibility, there is need to search for coupled with potential harmful effects on the environ- more allelochemicals against borer weevils and testing ment and human health, which has necessitated the the effects when these and pheromones are com- search for sustainable alternatives to synthetic pesti- bined. In addition, the synergistic effects of combining cides. Nonetheless, these alternative management op- male aggregation pheromone with female sex phero- tions may also have their limitations that require further mone are other areas that could be exploited. research.

Use of plants with insecticidal properties Cultural methods • Several plant species have shown potentials to manage This first line of defense is widely applied in farms (e.g., C. sordidus with most tested families as Solanaceae, small-scale, commercial, or agro-industrial), and it is Asteraceae, and Meliaceae, but commercial products commonly integrated and compatible with other options. have been developed only from Meliaceae (e.g., neem Some practices such as mulching can attract or increase plant). activitiy of pest while others can have very slow action, and • Effects on C. sordidus are mainly of non-mortality type others such as classical trapping can be labor-intensive. (oviposition deterrence, feeding deterrence, repellen- Correspondingly, evidences from field experiments cy, reduction in size and weight, and decreased haemo- showed that the decrease of C. sordidus in living mulch cyte counts for weevils). plots does not affect corm damage and fruit yield. • Only Piper spp. was found to have high mortality for • Clean planting materials (the case of tissue culture) are adult weevils while only T. diversifolia and Phytolacca scarce and relatively expensive for small-scale farmers, spp. caused high mortality to eggs and larvae of which makes its adoption difficult. Hence, many of C sordidus. small-scale farmers are adopting macro-propagated • Piper spp. and S. aromaticum elicited very high repel- plants while some still rely on pared/unpared traditional lency—Class IV according to the International Orga- suckers. More research is needed to evaluate/compare nization for Biological Control (IOBC) standard.

http://www.cabi.org/cabreviews 16 CAB Reviews • Most of these potential botanical pesticides do not the field. Abera-Kalibata 202[ ] reported that ants are cause direct mortality to adults and many with high not able to provide economic control of banana wee- potentials have not been formulated as commercial vils under field conditions. products, and therefore not readily available for use by • Larvae and adults of the histerid —P. javanus farmers. was reported as the best predator on larvae and pu- • Although there are claims that these botanical pesti- pae of the pest. cides are environment-friendly, much still needs to be • Earwigs also reduce the population of C. sordidus by done to test their effects on non-target beneficial consuming eggs, larvae, and pupae. organisms in banana or plantain agroecosystems. • Most parasitoids and predators find it difficult to lo- ­Additionally, it is important to test the potencies of cate larvae and pupae that are usually found within extracts from the same plant species from different tunnels in residues that are usually blocked with frass agroecological zones. Also, more effort should be put or escavated plant materials. In addition, parasitism of to develop, test, and register commercial products weevil eggs is difficult since eggs are usually laid in from plants with proven potencies. holes in corms that are covered by the female weevils after oviposition. • Most of these generalist predators can also feed on Entomopathogens non-target beneficial soil-dwelling organisms. • More searches for indigenous parasitoids and preda- • The fungus Beauveria bassiana and nematodes Steiner- tors are needed to evaluate establishment and effec- nema spp. or Heterorhabditis spp. are widely used as tiveness of predators like P. javanus to other areas and effective entomopathogens for C. sordidus larvae and to determine the impact of other management op- adults. tions like entomopathogens, synthetic, and botanical • Like non-pathogenic fungi such as F. oxysporum and B. pesticides on natural enemies. bassiana also plays an important role as fungal endophyte. • Even though there are several strains of these entomo- Resistant varieties and genetic modification pathogens, relevant commercial products are scarce. Also, adult weevil mortality caused by these pathogens is • Generally, most plantains, East African Highland ba- more effective and enhanced only when they are applied nanas and hybrids are resistant to borer weevils with on pseudostem traps, disc-on-corm traps, and corm inci- antibiosis as the main resistance mechanism. sions or when they are integrated with pheromones. • Most susceptible varieties found with high quantities • Effectiveness of these fungal pathogens in the field var- of glucose, salicin, and 1,8-cineole. ies with the fungal strain, culture medium, variety of • Corm hardness and latex quantity/viscosity as factors Musa spp., climate, method of application, and duration that negatively affect egg hatchability and survivorship of storage. of first instars. • EPNs have broad pest-insect host range, rapidly kill • Some phytocystatins were reportedly deleterious to insect host, have active searching behavior using olfac- larvae of the pest. tory cues, can be mass produced in vivo and in vitro, • Find ways to engineer effective phytocystatins to de- safe for non-target organism with strong potential for velop resistant cultivars to borer weevils. use in integrated pest management [245]. EPNs can penetrate C. sordidus larval galleries and easily reproduce, while weevil mortality varies with the EPN species Acknowledgement and concentration. • It is necessary to formulate commercial products Dr. Woin Noe, the Director of IRAD/CARBAP Cameroon from the most effective EPN strains and test their ef- for permission to use all documents having information on ficacies under field conditions, and determine their banana borer weevil’s research. Dr. Sama Lang Patrick, soil compatibility with commercial pesticides. scientist and former Chief of CARBAP Antenna, Ekona, SW Region Cameroon, for the useful discussions and Predators and parasitoids provision of some literature. The members of pestnet@ yahoogroups.com (www.pestnet.org) for the information • Although successful parasitoids have not been identi- exchanges and supply of literature. The administration of fied, generalist predators have been recorded with PRAM Martinique for hosting the first author in 2009 and many having limited potential to manage the pest, and therefore facilitating access to numerous literatures on C. only toads were found consuming adult weevils. sordidus. Dr. Christopher Mbua Parr, former Research • Some ant species (Odontomachus spp., Tetramorium Manager, Cameroon Development Corporation (CDC) spp., and P. megacephalia) were found with best preda- Banana plantation for providing useful literature as well as tion results for eggs, larvae, and pupae of C. sordidus in working with the first author on many field experiments.

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